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Compensatory ion transport buffers daily protein rhythms to regulate osmotic balance and cellular physiology

Author

Listed:
  • Alessandra Stangherlin

    (MRC Laboratory of Molecular Biology)

  • Joseph L. Watson

    (MRC Laboratory of Molecular Biology)

  • David C. S. Wong

    (MRC Laboratory of Molecular Biology)

  • Silvia Barbiero

    (MRC Laboratory of Molecular Biology)

  • Aiwei Zeng

    (MRC Laboratory of Molecular Biology)

  • Estere Seinkmane

    (MRC Laboratory of Molecular Biology)

  • Sew Peak Chew

    (MRC Laboratory of Molecular Biology)

  • Andrew D. Beale

    (MRC Laboratory of Molecular Biology)

  • Edward A. Hayter

    (University of Manchester)

  • Alina Guna

    (UCSF)

  • Alison J. Inglis

    (California Institute of Technology)

  • Marrit Putker

    (MRC Laboratory of Molecular Biology
    Crown Bioscience Netherlands B.V.)

  • Eline Bartolami

    (University of Geneva
    CEA, IRIG, SyMMES)

  • Stefan Matile

    (University of Geneva)

  • Nicolas Lequeux

    (Sorbonne Université)

  • Thomas Pons

    (Sorbonne Université)

  • Jason Day

    (University of Cambridge)

  • Gerben van Ooijen

    (University of Edinburgh)

  • Rebecca M. Voorhees

    (California Institute of Technology)

  • David A. Bechtold

    (University of Manchester)

  • Emmanuel Derivery

    (MRC Laboratory of Molecular Biology)

  • Rachel S. Edgar

    (Imperial College London)

  • Peter Newham

    (Clinical Pharmacology and Safety Sciences, R&D, AstraZeneca)

  • John S. O’Neill

    (MRC Laboratory of Molecular Biology)

Abstract

Between 6–20% of the cellular proteome is under circadian control and tunes mammalian cell function with daily environmental cycles. For cell viability, and to maintain volume within narrow limits, the daily variation in osmotic potential exerted by changes in the soluble proteome must be counterbalanced. The mechanisms and consequences of this osmotic compensation have not been investigated before. In cultured cells and in tissue we find that compensation involves electroneutral active transport of Na+, K+, and Cl− through differential activity of SLC12A family cotransporters. In cardiomyocytes ex vivo and in vivo, compensatory ion fluxes confer daily variation in electrical activity. Perturbation of soluble protein abundance has commensurate effects on ion composition and cellular function across the circadian cycle. Thus, circadian regulation of the proteome impacts ion homeostasis with substantial consequences for the physiology of electrically active cells such as cardiomyocytes.

Suggested Citation

  • Alessandra Stangherlin & Joseph L. Watson & David C. S. Wong & Silvia Barbiero & Aiwei Zeng & Estere Seinkmane & Sew Peak Chew & Andrew D. Beale & Edward A. Hayter & Alina Guna & Alison J. Inglis & Ma, 2021. "Compensatory ion transport buffers daily protein rhythms to regulate osmotic balance and cellular physiology," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-25942-4
    DOI: 10.1038/s41467-021-25942-4
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    References listed on IDEAS

    as
    1. Alexander C. West & Laura Smith & David W. Ray & Andrew S. I. Loudon & Timothy M. Brown & David A. Bechtold, 2017. "Misalignment with the external light environment drives metabolic and cardiac dysfunction," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    2. Mohammad U. Zahid & Liang Ma & Sung Jun Lim & Andrew M. Smith, 2018. "Single quantum dot tracking reveals the impact of nanoparticle surface on intracellular state," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    3. Edward A. Hayter & Sophie M. T. Wehrens & Hans P. A. Dongen & Alessandra Stangherlin & Shobhan Gaddameedhi & Elena Crooks & Nichola J. Barron & Luigi A. Venetucci & John S. O’Neill & Timothy M. Brown , 2021. "Distinct circadian mechanisms govern cardiac rhythms and susceptibility to arrhythmia," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    4. J. Wade Harper & Eric J. Bennett, 2016. "Proteome complexity and the forces that drive proteome imbalance," Nature, Nature, vol. 537(7620), pages 328-338, September.
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    Cited by:

    1. Enrico Pracucci & Robert T. Graham & Laura Alberio & Gabriele Nardi & Olga Cozzolino & Vinoshene Pillai & Giacomo Pasquini & Luciano Saieva & Darren Walsh & Silvia Landi & Jinwei Zhang & Andrew J. Tre, 2023. "Daily rhythm in cortical chloride homeostasis underpins functional changes in visual cortex excitability," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Leonard L. Boer & Lesley Vanes & Serena Melgrati & Joshua Biggs O’May & Darryl Hayward & Paul C. Driscoll & Jason Day & Alexander Griffiths & Renata Magueta & Alexander Morrell & James I. MacRae & Rob, 2023. "T cell migration requires ion and water influx to regulate actin polymerization," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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